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<article xmlns:mml="http://www.w3.org/1998/Math/MathML" xmlns:xlink="http://www.w3.org/1999/xlink" dtd-version="1.3" xml:lang="en" article-type="brief-report"><?properties open_access?><processing-meta base-tagset="archiving" mathml-version="3.0" table-model="xhtml" tagset-family="jats"><restricted-by>pmc</restricted-by></processing-meta><front><journal-meta><journal-id journal-id-type="nlm-ta">Emerg Infect Dis</journal-id><journal-id journal-id-type="iso-abbrev">Emerg Infect Dis</journal-id><journal-id journal-id-type="publisher-id">EID</journal-id><journal-title-group><journal-title>Emerging Infectious Diseases</journal-title></journal-title-group><issn pub-type="ppub">1080-6040</issn><issn pub-type="epub">1080-6059</issn><publisher><publisher-name>Centers for Disease Control and Prevention</publisher-name></publisher></journal-meta><article-meta><article-id pub-id-type="pmid">35319434</article-id><article-id pub-id-type="pmc">8962908</article-id><article-id pub-id-type="publisher-id">21-2243</article-id><article-id pub-id-type="doi">10.3201/eid2804.212243</article-id><article-categories><subj-group subj-group-type="heading"><subject>Research Letter</subject></subj-group><subj-group subj-group-type="article-type"><subject>Research Letter</subject></subj-group><subj-group subj-group-type="TOC-title"><subject>Spread of SARS-CoV-2 Variants on R&#x000e9;union Island, France, 2021</subject></subj-group></article-categories><title-group><article-title>Spread of SARS-CoV-2 Variants on R&#x000e9;union Island, France, 2021</article-title><alt-title alt-title-type="running-head">Spread of SARS-CoV-2 Variants on R&#x000e9;union Island, France, 2021</alt-title></title-group><contrib-group><contrib contrib-type="author"><name><surname>Mercier</surname><given-names>Aliz&#x000e9;</given-names></name></contrib><contrib contrib-type="author"><name><surname>Wilkinson</surname><given-names>David A.</given-names></name></contrib><contrib contrib-type="author"><name><surname>Lebarbenchon</surname><given-names>Camille</given-names></name></contrib><contrib contrib-type="author"><name><surname>Mavingui</surname><given-names>Patrick</given-names></name></contrib><contrib contrib-type="author" corresp="yes"><name><surname>Yemadje-Menudier</surname><given-names>Luce</given-names></name></contrib><aff id="aff1">Sant&#x000e9; Publique France, Saint-Denis, France (A. Mercier, L. Yemadje-Menudier); </aff><aff id="aff2">Universit&#x000e9; de La R&#x000e9;union, Centre National de la Recherche Scientifique, Institut National de la Sant&#x000e9; et de la Recherche M&#x000e9;dicale, Institut de Recherche pour le D&#x000e9;veloppement, Sainte-Clotilde, France (D.A. Wilkinson, C. Lebarbenchon, P. Mavingui); </aff><aff id="aff3">Plateforme Technologique du Cyclotron R&#x000e9;union Oc&#x000e9;an Indien (CYROI), Sainte-Clotilde (D.A. Wilkinson)</aff></contrib-group><author-notes><corresp id="cor1">Address for correspondence: Luce Yemadje-Menudier, Sant&#x000e9; Publique France&#x02014;R&#x000e9;union Island, 2 bis avenue Georges Brassens, 97408 Saint-Denis CEDEX 9, La R&#x000e9;union, France; email: <email xlink:href="luce.menudier@santepubliquefrance.fr">luce.menudier@santepubliquefrance.fr</email></corresp></author-notes><pub-date pub-type="ppub"><month>4</month><year>2022</year></pub-date><volume>28</volume><issue>4</issue><fpage>895</fpage><lpage>898</lpage><permissions><copyright-year>2022</copyright-year><license><ali:license_ref xmlns:ali="http://www.niso.org/schemas/ali/1.0/" specific-use="textmining" content-type="ccbylicense">https://creativecommons.org/licenses/by/4.0/</ali:license_ref><license-p>Preventing Chronic Disease is a publication of the U.S. Government. This publication is in the public domain and is therefore without copyright. All text from this work may be reprinted freely. Use of these materials should be properly cited.</license-p></license></permissions><abstract><p>In January 2021, after detection of severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) variants, genomic surveillance was established on R&#x000e9;union Island to track the introduction and spread of SARS-CoV-2 lineages and variants of concern. This system identified 22 SARS-CoV-2 lineages, 71% of which were attributed to the Beta variant</p></abstract><kwd-group kwd-group-type="author"><title>Keywords: </title><kwd>COVID-19</kwd><kwd>SARS-CoV-2</kwd><kwd>severe acute respiratory syndrome coronavirus 2</kwd><kwd>viruses</kwd><kwd>respiratory infections</kwd><kwd>zoonoses</kwd><kwd>epidemiology</kwd><kwd>sequencing</kwd><kwd>variants</kwd><kwd>France</kwd><kwd>R&#x000e9;union Island</kwd></kwd-group><kwd-group kwd-group-type="author"><kwd><italic>Suggested citation for this article</italic>: Mercier A</kwd><kwd>Wilkinson DA</kwd><kwd>Lebarbenchon C</kwd><kwd>Mavingui P</kwd><kwd>Yemadje-Menudier L. Spread of SARS-CoV-2 variants on R&#x000e9;union Island</kwd><kwd>France</kwd><kwd>2021. Emerg Infect Dis. 2022 Apr [<italic>date cited</italic>]. <ext-link xlink:href="https://doi.org/10.3201/eid2804.212243" ext-link-type="uri">https://doi.org/10.3201/eid2804.212243</ext-link></kwd></kwd-group></article-meta></front><body><p>Coronavirus disease (COVID-19) is a respiratory illness caused by severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2). On R&#x000e9;union Island, an overseas department of France located in the Indian Ocean, the first cases of COVID-19 were detected on March 11, 2020, in a group of travelers (D.A. Wilkinson et al., unpub. data, <ext-link xlink:href="https://doi.org/10.1101/2021.01.21.21249623" ext-link-type="uri">https://doi.org/10.1101/2021.01.21.21249623</ext-link>). In response, a regional epidemiologic surveillance focusing on contact tracing and early detection of clusters was conducted. After several months of imported cases and sporadic autochtonous cases, a sharp increase in locally acquired infections was recorded in August 2020, after the return of many R&#x000e9;union Island residents from travel abroad, primarily mainland France, where the incidence rate was high. The virus subsequently spread throughout the island.</p><p>In January 2021, after SARS-CoV-2 variants were detected, genomic surveillance was established to track the introduction and spread of SARS-CoV-2 lineages on the island. During January&#x02013;June 2021, we generated a total of 1,528 genome sequences with <underline>&#x0003e;</underline>90% coverage using the ARTIC protocol (https://artic.network/ncov-2019/ncov2019-bioinformatics-sop.html) and nanopore technology (MinION; Oxford Nanopore Technologies, <ext-link xlink:href="https://nanoporetech.com" ext-link-type="uri">https://nanoporetech.com</ext-link>). This collection represents 8.3% of all COVID-19 cases on R&#x000e9;union Island during that period (n = 18,409). Sample selection was pseudo-random; a small proportion of cases was prioritized for sequencing because of atypical epidemiologic or clinical characteristics. Pangolin lineages were assigned to all genomes using Pangolin version 1.2.88 (<ext-link xlink:href="https://github.com/cov-lineages/pango-designation/releases/tag/v1.2.88" ext-link-type="uri">https://github.com/cov-lineages/pango-designation/releases/tag/v1.2.88</ext-link>).</p><p>We present the main findings of genomic surveillance from weeks 1&#x02013;22, 2021 (January 4&#x02013;June 6, 2021). We focused on the evolution of the weekly proportions of the 8 most frequent SARS-CoV-2 variants and examined the correlation between the weekly number of confirmed cases and the proportion of sequences identified as Beta variant (B.1.351). We extracted lineage distributions in other islands of the Indian Ocean and South Africa from the GISAID database (<ext-link xlink:href="http://www.gisaid.org" ext-link-type="uri">http://www.gisaid.org</ext-link>) to investigate the origins of the Beta variant sublineages.</p><p>We identified 22 SARS-CoV-2 lineages, 71% of which were attributed to the Beta variant (sublineages B.1.351 and B.1.351.2) (<xref rid="T1" ref-type="table">Table</xref>). On the basis of available data in the GISAID database, lineage B.1.622 seems to be specific to R&#x000e9;union Island; no other sequence had been reported elsewhere.</p><table-wrap position="float" id="T1"><label>Table</label><caption><title>Observed lineages of severe acute respiratory syndrome coronavirus 2, R&#x000e9;union, France, 2021</title></caption><table frame="hsides" rules="groups"><col width="163" span="1"/><col width="74" span="1"/><thead><tr><th valign="bottom" align="left" scope="col" rowspan="1" colspan="1">Pangolin lineage</th><th valign="bottom" align="center" scope="col" rowspan="1" colspan="1">No. genomes</th></tr></thead><tbody><tr><td valign="middle" align="left" scope="row" rowspan="1" colspan="1">B.1.351.2 (Beta, sub-lineage 2)</td><td valign="middle" align="center" rowspan="1" colspan="1">716</td></tr><tr><td valign="middle" align="left" scope="row" rowspan="1" colspan="1">B.1.351 (Beta, sub-lineage 0)</td><td valign="middle" align="center" rowspan="1" colspan="1">361</td></tr><tr><td valign="middle" align="left" scope="row" rowspan="1" colspan="1">B.1.177</td><td valign="middle" align="center" rowspan="1" colspan="1">154</td></tr><tr><td valign="middle" align="left" scope="row" rowspan="1" colspan="1">B.1.622</td><td valign="middle" align="center" rowspan="1" colspan="1">71</td></tr><tr><td valign="middle" align="left" scope="row" rowspan="1" colspan="1">B.1.1.7 (Alpha)</td><td valign="middle" align="center" rowspan="1" colspan="1">65</td></tr><tr><td valign="middle" align="left" scope="row" rowspan="1" colspan="1">B.1.160</td><td valign="middle" align="center" rowspan="1" colspan="1">55</td></tr><tr><td valign="middle" align="left" scope="row" rowspan="1" colspan="1">B.1.160.18</td><td valign="middle" align="center" rowspan="1" colspan="1">36</td></tr><tr><td valign="middle" align="left" scope="row" rowspan="1" colspan="1">B.1.1.353</td><td valign="middle" align="center" rowspan="1" colspan="1">18</td></tr><tr><td valign="middle" align="left" scope="row" rowspan="1" colspan="1">B.1.617.2 (Delta)</td><td valign="middle" align="center" rowspan="1" colspan="1">14</td></tr><tr><td valign="middle" align="left" scope="row" rowspan="1" colspan="1">B.1.438.2</td><td valign="middle" align="center" rowspan="1" colspan="1">10</td></tr><tr><td valign="middle" align="left" scope="row" rowspan="1" colspan="1">B.1.525 (Eta)</td><td valign="middle" align="center" rowspan="1" colspan="1">8</td></tr><tr><td valign="middle" align="left" scope="row" rowspan="1" colspan="1">B.1.416.1</td><td valign="middle" align="center" rowspan="1" colspan="1">5</td></tr><tr><td valign="middle" align="left" scope="row" rowspan="1" colspan="1">B.1.177.24</td><td valign="middle" align="center" rowspan="1" colspan="1">3</td></tr><tr><td valign="middle" align="left" scope="row" rowspan="1" colspan="1">B.1</td><td valign="middle" align="center" rowspan="1" colspan="1">3</td></tr><tr><td valign="middle" align="left" scope="row" rowspan="1" colspan="1">B.1.177.37</td><td valign="middle" align="center" rowspan="1" colspan="1">2</td></tr><tr><td valign="middle" align="left" scope="row" rowspan="1" colspan="1">B.1.1</td><td valign="middle" align="center" rowspan="1" colspan="1">1</td></tr><tr><td valign="middle" align="left" scope="row" rowspan="1" colspan="1">B.1.1.241</td><td valign="middle" align="center" rowspan="1" colspan="1">1</td></tr><tr><td valign="middle" align="left" scope="row" rowspan="1" colspan="1">B.1.160.27</td><td valign="middle" align="center" rowspan="1" colspan="1">1</td></tr><tr><td valign="middle" align="left" scope="row" rowspan="1" colspan="1">B.1.177.81</td><td valign="middle" align="center" rowspan="1" colspan="1">1</td></tr><tr><td valign="middle" align="left" scope="row" rowspan="1" colspan="1">B.1.221</td><td valign="middle" align="center" rowspan="1" colspan="1">1</td></tr><tr><td valign="middle" align="left" scope="row" rowspan="1" colspan="1">B.1.428.2</td><td valign="middle" align="center" rowspan="1" colspan="1">1</td></tr><tr><td valign="middle" align="left" scope="row" rowspan="1" colspan="1">P.2<hr/></td><td valign="middle" align="center" rowspan="1" colspan="1">1<hr/></td></tr><tr><td valign="middle" align="left" scope="row" rowspan="1" colspan="1">Total</td><td valign="middle" align="center" rowspan="1" colspan="1">1,528</td></tr></tbody></table></table-wrap><p>The Beta variant was first detected on R&#x000e9;union Island during the first week of January 2021, although it may have been introduced before its detection by full-genome sequencing. During the first 6 weeks of 2021, lineages known to have high levels of circulation in Europe (e.g., B.1.160, B.1.177) represented most sequenced genomes (<xref rid="F1" ref-type="fig">Figure</xref>). This finding highlights the strong effect of air travel on COVID-19 dynamics on an island such as R&#x000e9;union (<xref rid="R1" ref-type="bibr"><italic>1</italic></xref>; D.A. Wilkinson et al., unpub. data).</p><fig position="float" id="F1" fig-type="figure"><label>Figure</label><caption><p>A) Epidemic curve of severe acute respiratory syndrome coronavirus 2cases detected in R&#x000e9;union, France by week of sampling, weeks 1&#x02013;22, 2021. Orange bars correspond to school holidays. B) Distribution of severe acute respiratory syndrome coronavirus 2 lineages identified in R&#x000e9;union, France. Weekly number of sequenced genomes appears above the relevant bar. </p></caption><graphic xlink:href="21-2243-F" position="float"/></fig><p>Since mid-February 2021 (week 7 of 2021), the Beta variant has become dominant on R&#x000e9;union Island, despite low-level circulation of the Alpha variant, another variant of concern that was dominant in mainland France and other countries in Europe at that time. We detected a correlation (Spearman &#x003c1;&#x000a0;=&#x000a0;8.4 &#x000d7; 10<sup>&#x02212;4</sup>; p&#x0003c;0.001) between the number of COVID-19 cases in January&#x02013;February 2021 and the number of sequences attributed to the Beta variant, which has been shown to have increased transmissibility (C.A. Pearson et al., unpub. data, <ext-link xlink:href="https://cmmid.github.io/topics/covid19/sa-novel-variant.html" ext-link-type="uri">https://cmmid.github.io/topics/covid19/sa-novel-variant.html</ext-link>). Several additional factors could explain the dominance of Beta variant; genetic and epidemiologic factors may have contributed to a founder effect, a higher frequency of virus introductions resulting from holiday travels, possible superspreading events, and local and regional contexts (<xref rid="R2" ref-type="bibr"><italic>2</italic></xref>). Indeed, geographic proximity and population movements with Mayotte, another overseas department of France, and Comoros link R&#x000e9;union Island to South Africa, where Beta variant was first reported (<xref rid="R3" ref-type="bibr"><italic>3</italic></xref>).</p><p>We detected 2 sublineages of Beta variant, B.1.351 and B.1.351.2. Sublineage B.1.351.2 accounted for 3-fold more cases than B.1.351. It was detected concurrently in Mayotte, Comoros, and R&#x000e9;union Island. This finding, coupled with information from GISAID, suggests that lineage B.1.351.2 was imported to Comoros and Mayotte from South Africa and could have been introduced to R&#x000e9;union Island from Mayotte (<xref rid="R4" ref-type="bibr"><italic>4</italic></xref>) (<xref rid="SD1" ref-type="supplementary-material">Appendix 1</xref>). This possible introduction from Mayotte is supported by the flow of travelers between the 2 departments and the notable peak in COVID-19 cases that occurred in Mayotte during weeks 1&#x02013;11, mainly caused by the Beta variant (<xref rid="R5" ref-type="bibr"><italic>5</italic></xref>). However, analysis of the origin of lineages is strongly affected by each location&#x02019;s capacity to sequence and report genomes in GISAID, which renders comparison between different locations difficult (<xref rid="R4" ref-type="bibr"><italic>4</italic></xref>).</p><p>Our study provides valuable insights into the interactions between SARS-CoV-2 lineages on R&#x000e9;union Island, which represents a closed system with controlled entries, especially when travel restrictions are in place. Additional research on genomic epidemiology and the effect of air travel can further improve understanding of why some variants become dominant over others, particularly in insular contexts. The future of genomic surveillance on R&#x000e9;union Island will focus on mutation screening to increase reactivity, combined with real-time sequencing, as a robust approach to track the spread of emerging SARS-CoV-2 variants of concern and to inform public health actions (<xref rid="R6" ref-type="bibr"><italic>6</italic></xref>,<xref rid="R7" ref-type="bibr"><italic>7</italic></xref>).</p><supplementary-material id="SD1" position="float" content-type="local-data"><caption><title>Appendix 1</title><p>Additional information from study of the spread of severe acute respiratory syndrome coronavirus 2 variants on the island of R&#x000e9;union, France 2021.</p></caption><media xlink:href="21-2243-Techapp-s1.pdf" id="d64e322" position="anchor"/></supplementary-material><supplementary-material id="SD2" position="float" content-type="local-data"><caption><title>Appendix 2</title><p>Information about severe acute respiratory syndrome coronavirus 2 sequences obtained from GISAID in study of variants on the island of R&#x000e9;union, France, 2021.</p></caption><media xlink:href="21-2243-Techapp-s2.xlsx" id="d64e327" position="anchor"/></supplementary-material></body><back><ack><title>Acknowledgments </title><p>We thank all the partners involved in the surveillance of COVID-19 in the Regional Health Agency and the Regional Health Insurance Fund. We acknowledge the key role of the network of sampling laboratories on R&#x000e9;union Island (CHU, CHOR, Laboratoire de Saint-Benoit, Bioaustral, R&#x000e9;unilab, Cerballiance). We also acknowledge and thank the members of the EMERGEN consortium, as well as Laetitia Ali Oicheih, Elsa Balleydier, Adeline Feri, Javier Castro Alvarez, Sibylle Bernard-Stoecklin, Anna Maisa, Justine Schaeffer, Bruno Coignard, Guillaume Spaccaferri, Bruno Lina, Marie-Alice Simbi, Magali Turpin, Christian M&#x000e9;riau, and Maya Cesari. We are also grateful to the originating and submitting laboratories of the sequences from GISAID database (<xref rid="SD1" ref-type="supplementary-material">Appendix 2</xref>). All data submitters may be contacted via the GISAID website (<ext-link xlink:href="https://www.gisaid.org" ext-link-type="uri">https://www.gisaid.org</ext-link>).</p></ack><bio id="d64e339"><p>Dr. Mercier is an epidemiologist at Sant&#x000e9; publique France, based in the regional office of R&#x000e9;union. She has a PhD in epidemiology specialized in epidemic intelligence. Her research interests include infectious disease epidemiology, epidemic intelligence, and modeling.</p></bio><ref-list><title>References</title><ref id="R1"><label>1. </label><mixed-citation publication-type="webpage"><string-name><surname>O&#x02019;Toole</surname>
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